Light-driven host-symbiont interactions under hosts’ range shifts caused by global warming: A review

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Light-driven host-symbiont interactions under hosts’ range shifts caused by global warming: A review A.M. Markkolaa,* , K. Saravesia , S. Aikiob , E. Taulavuoria , K. Taulavuoria a b

Department of Ecology, University of Oulu, POB 3000, FI-90014, Finland Finnish Museum of Natural History LUOMUS, POB 7, FI-00014 University of Helsinki, Finland

A R T I C L E I N F O

A B S T R A C T

Article history: Received 28 February 2015 Received in revised form 22 May 2015 Accepted 23 May 2015 Available online xxx

The spectrum of light has received little attention as an ecological factor and in this review we highlight the importance of a changing light environment in plant range shifts under conditions of global warming. Although distinct clinal responses to light quality have not been earlier reported, some studies have shown that northern ecotypes are more sensitive to changes in light quality. The northern light environment may significantly modify competition between plant species and within photoperiodic ecotypes, if predicted rapid range shifts of forest trees are realized. Southern photoperiodic ecotypes of forest trees migrating northward will encounter both changed light quality and a different photoperiod. Our special focus is on carbon economy and biomass partitioning between the autotrophic hosts and heterotrophic ectomycorrhizal fungal (EMF) symbionts, reciprocally dependent on each other. This applies also to the level of fungal community structure, which is assumed to be determined in part by host carbon economy. We hypothesize, that (1) Carbon allocation to roots and EMF in different host species and locally adapted photoperiodic ecotypes will respond differentially to northern light climate, especially to photoperiod and proportionally higher diffuse blue light; (2) Since carbon flux belowground may start later in northward-shifted southern populations in the autumn, also mycelial growth and reproduction in the EMF associated with southern populations could occur later. This may also lead to changes in fungal community composition; (3) EMF phenology and community composition may show different responses to changing light climate when associated with host trees of fixed or free growth pattern; and (4) Responses of EMF symbionts associated with locally adapted host populations vary, possibly leading to changes in EMF communities. We also discuss potential experimental approaches mimicking range shift conditions in terms of light quality due to global warming and compare reaction norms in key traits between southern and northern populations and species. Further, we exemplify how data obtained from experimental studies may be used for modelling of host plant and symbiont growth, which may in turn affect species competitive ability and distribution. ã2015 Published by Elsevier B.V.

Key words: Light quality Climate change Seasonality Host carbon flux Biomass allocation Boreal forest trees Ectomycorrhizal fungal symbionts Photoperiodic ecotypes

1. Introduction Global climate change has provoked serious discussion about near-future impacts on ecosystem services and biodiversity (e.g. Hautier et al., 2014; Martin et al., 2014). This is of special importance in boreal and arctic ecosystems because of the predicted rapid changes in these areas (ACIA, 2005). Increased attention directed toward northern areas encompasses problems associated with invasion ecology and range shifts of species and their populations (Saikkonen et al., 2012; Taulavuori, 2013; Leiblein-Wild and Tackenberg, 2014). Light environment, and

* Corresponding author. Tel.: +358 294 481530. E-mail address: Annamari.Markkola@oulu.fi (A.M. Markkola).

especially differences in the spectrum of light, as an ecological factor, however, has received little attention in this respect. Here we address certain key questions related to global warming and consequent interactions of dominant forest trees species, their populations adapted to local light environment (i.e. ecotypes), and their ectomycorrhizal fungal (EMF) symbionts under host range shifts towards the northern light environment, where blue light is enriched (Taulavuori et al., 2010). The special focus is on carbon economy and biomass partitioning between an autotrophic host and heterotrophic fungal symbionts, but this applies also to the level of fungal community structure, which is assumed to be determined in part by host carbon economy. The host tree–fungal symbiont pair interaction is of specific interest, as EMF symbionts consume a substantial proportion of the net carbon fixed by the host, but may also significantly aid host adaptation to a

http://dx.doi.org/10.1016/j.envexpbot.2015.05.009 0098-8472/ ã 2015 Published by Elsevier B.V.

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changing environment due to their distinctly shorter life span and high diversity compared to their host trees. 2. Light environment and growth patterns of boreal forest trees 2.1. Importance of light Light is probably the most important resource plants compete for (e.g. Schwinning and Weiner, 1998). Light intensity (irradiance) determines photosynthetic potential until the level of saturation, and thereby net primary production. Light quality (spectral composition) affects plant phenotype through many photomorphogenic processes, and acts as a signal for metabolic regulation (Cashmore, 2006). Light duration (daylength, photoperiod) is responsible for adjusting biological clock for phenological events (Thomas and Vince-Prue, 1997). Changes in any of these characteristics of a plant’s light environment can cue phenological transitions, such as flowering and seed germination, and determine biomass partitioning between foliage, roots and supporting tissues, as well as the allocation of photosynthates to symbiotic partners. Impacts of future climate change on vegetation have attracted considerable interest during past years. Increases in plant growth due to global warming and elevated CO2 are welldocumented (Bazzaz, 1990). Such impacts on EMF symbionts of trees and shrubs have also been reviewed (Pickles et al., 2012; Morgado et al., 2015). In contrast, the light environment has been largely neglected in this context. It is therefore crucial to investigate how forest trees respond to changes in light climate when migrating to the north along with climate warming. 2.2. Northern light environment The light environment at northern high latitudes is markedly different from the mid latitudes and likely to affect plant competitive performance during the growing season. Day length begins to extend from the winter solstice at a rate that increases until the vernal equinox, being 12 h on the 20th March, and reaching 24 h (i.e. polar day) at a diminishing rate by the summer solstice around the 21st June at the Arctic Circle (66.56
N) and northwards, and lasting for two months at 70
N (Nilsen, 1985; Taulavuori et al., 2010). In addition to the missing darkness during the growing season, the light environment in the north is characterized by lower light intensity (irradiance) compared to mid or low latitudes. For example, vegetation around the Arctic Circle in Scandinavia receives only about 55% of the irradiance of that in the Alps (47
N) (Körner, 2003). Moreover, light quality is different since the polar summer nights are enriched with a relatively high proportion of diffuse blue because of the light scattering due to the low angle of solar radiation (Taulavuori et al., 2010). 2.3. Day length impacts on phenology of trees Day length is the most accurate and consistent environmental cue in northernmost environments, providing a fixed calendar for plant seasonality, which is especially important for plant preparation for winter (e.g. Taulavuori et al., 1997; E. Taulavuori et al., 2010; Saikkonen et al., 2012; Taulavuori, 2013). Weather conditions (temperature, precipitation) are too unpredictable to provide reliable signals for autumn preparation, and can therefore only fine-tune plant seasonality (e.g. Taulavuori et al., 1997; Taulavuori, 2006; Rohde et al., 2011). Hence, many phenological events are coordinated by day length. Pattern of shoot elongation characterizes tree species. Trees with a free growth pattern have shoots that elongate producing new internodes throughout the growing season until a critical

photoperiod. The final length of the shoot is determined by prevailing weather conditions. In trees with a fixed (predetermined) growth pattern, the weather conditions of the previous growing season determine the number of internodes in the bud. Elongation of internodes in these species is controlled by temperature of the next growing season (e.g. Kramer and Kozlowski, 1979; Junttila, 2007). The elongation in fixed growth pattern plants occurs during a relatively short period in the beginning of the growing season elongation is then followed by needle and diameter growth, apical bud set and subsequent frost hardening processes. Shortening days induce winter hardening of trees irrespective of growth pattern (e.g. Sakai and Larcher, 1987; Taulavuori et al., 1997). In addition, temperature signals may contribute to the timing of photoperiod growth cessation (Rohde et al., 2011). It is also proposed that the signal function of annual change in photoperiod is replaced by changes in light quality in the high Arctic (78
N), where midnight sun continues until leaf shedding, and thus cannot provide a signal for growth cessation (Nilsen, 1985). Nilsen (1985) proposed that a reduction in the ratio of red to far-red light (R:FR) may provide an alternative signal, analogous to an increase in blue to red light ratio (Taulavuori et al., 2010), in the context of reduced elongation of many species growing in the light of subarctic polar summer (Taulavuori et al., 2005; Sarala et al., 2007, 2011). 2.4. Adaptations to local light environment under range shifts Responses to photoperiod may vary to such an extent, that populations within a tree species could form so-called phototoperiodic ecotypes, which are genetically differentiated (Oleksyn et al., 1998; Junttila, 2007). This is typical for northern species (e.g. Betula spp.), which exhibit clinal adaptation over latitudes, indicating that the critical day length for growth cessation increases with increasing latitude of a population (Junttila, 2007; and references therein). Interestingly, adaptation to local photoperiodic conditions seems to differ also within tree species, e.g. certain woody species in the Rosaceae family do not show such clinal variation (Heide and Prestrud, 2005). Although distinct clinal responses to light quality has not been reported yet, some studies have shown that northern ecotypes are more sensitive to changes in light quality (e.g. Mølmann et al., 2006; Sarala et al., 2011). Northern light environment may thus significantly modify the competition between plant species and photoperiodic ecotypes, if predicted rapid range shifts of forest trees are realized (Taulavuori et al., 2013). In a century, estimated shift distances are in the range of 300–800 km (McKenney et al., 2007), and species ranges may shift northward as much as 1000 km (ACIA, 2005). In Finland, for example, a shift of this magnitude approaches the full latitudinal range of the boreal forest in this region and is similar to a transition from southern provenances to the most northern provenances, i.e. close to the Arctic Sea which prevents further shifts towards the north. Shift predictions vary among forest tree species due to different populations and genotypes, which may possess contrasting adaptation to local climate (Savolainen et al., 2007; Kremer et al., 2012; see Fig. 1). When considering northward range shifts of plant populations, temperature is the most efficient ecological filter against the shifts. In practice, under a rapidly warming climate, temperature will shift first and vegetation is expected to follow. Thus, populations shifting northwards will experience no change in temperature, while they experience a significantly different light environment (Taulavuori et al., 2010, 2013). This is most pronounced in boreal forest trees with a long generation age. Different ecotypes will therefore exhibit characteristic responses to the existing new light environment. While temperature signals may contribute to the timing of photoperiod growth cessation

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Fig. 1. Global warming challenges vegetation to adapt to higher temperatures, but also allows range shifts (colonization) northwards. A local northern (N) population has to cope with changes in temperature while colonized southern (S) species/ population has to respond to a changed light environment (photoperiod, light quality). Before climate change, both N and S populations are adapted to both the temperature and light environment of their respective ranges. After climate change competition is predicted to take place between N populations that are adapted to the northern light environment but not to the increased temperature, and S populations that are adapted to higher temperatures but not the northern light environment. There are currently no studies that could predict the outcome of the changed competition between northern and southern populations.

(Rohde et al., 2011), it concerns only deviations from optimal temperature (which is not changed during range shift). Principally, vegetation will track environmental changes with a time lag that reflects species limitations in their ability to disperse to and colonize new areas. The establishment of a species in a new area may therefore require several introduction attempts and local adaptation, which have been suggested as mechanisms behind the commonly observed time lags in species invasions (Aikio et al., 2010). In addition, currently existing vegetation of the north may inhibit and delay new colonizations. However, in managed forests, cultural areas and especially presently treeless tundra areas converting to forests, global warming will allow planting and sowing of more southern provenances and economically important tree species in northern areas. This will greatly speed up changes in forest vegetation and forest soils compared to natural dynamics. According to ACIA (2005), boreal forests will replace heath vegetation in tundra areas, which will be forced to shift towards the current polar desert. The present tundra ecotone will therefore be the actual battleground between northern and southern species and between populations. Acclimation and adaptation to the arctic light environment will be the key determinant in this competition (Taulavuori et al., 2010). 3. Significance of photosynthetic carbon flow for mycorrhizal fungi All northern forest trees form mutualistic ectomycorrhizal fungal (EMF) symbiosis in their fine roots, where resources are bilaterally exchanged between the plant and fungal partners. Carbon acquisition of EMF symbionts mainly depends on continuous flow of currently fixed photosynthates, which are quickly transferred from the autotrophic host to EMF (e.g. Högberg et al., 2001, 2008). A substantial proportion, 20–30% of net photosynthetic products is allocated to EMF (Finlay and Söderström, 1992; Markkola et al., 1995; Leake et al., 2004; Hobbie and Hobbie, 2006). Host photosynthesis is enhanced by EMF colonization which partially compensates for the increased carbon sink below ground (Dosskey et al., 1990). On the other hand, forest trees

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depend on EMF for nutrient acquisition. Most nutrients in acidic and cool northern soils are present in recalcitrant organic forms, which are mainly inaccessible for direct plant uptake but readily available for enzymatic hydrolysis/oxidation by soil fungi including EMF (Perez-Moreno and Read, 2000; Lindahl and Tunlid, 2015). Forest trees at high latitudes typically sustain very high levels of EMF colonization, which can also be regarded as an adaptation to low nutrient availability. The balance between energetic costs and nutritional benefits of mycorrhizal symbiosis may therefore change if a plant species disperses to a different light environment. Limited host carbon assimilation under an unfavourable light environment can be predicted to negatively affect EMF symbionts. Two general trends arise from host–symbiont interactions under varying carbon availability: firstly, fungal biomass production increases in high and decreases in low carbon conditions (Markkola et al., 2004; Treseder, 2004), and secondly, biomass of fungal symbionts seems to follow the growth responses of the host tree (Kirschbaum, 2000; Cudlin et al., 2007; Garcia et al., 2008; Saravesi et al., 2008; Andrew and Lilleskov, 2009). Generally, impaired carbon flow from the host tree, e.g. due to herbivory or girdling, has been shown to reduce growth and reproduction of EMF (Högberg et al., 2001; Kuikka et al., 2003; Markkola et al., 2004; Saravesi et al., 2008). Moreover, EMF species differ in terms of the amount of host-derived carbohydrates they require for growth and maintenance metabolism. Therefore, carbon limitation in trees often results in changes in EMF species composition rather than reduced overall EMF colonization (Saikkonen et al., 1999; Markkola et al., 2004; Saravesi et al., 2008, 2015; Ruotsalainen et al., 2009). Since EMF have differing modes of nutrient uptake, shifts in community composition of EMF will likely interact with host nutrition and growth. Timing differences of carbon allocation to shoot growth and potentially also to belowground sinks between trees with fixed and free growth patterns imply differences also in the seasonality of fungal biomass growth. 4. Biomass allocation between host tree and ectomycorrhizal fungi Optimal resource use theory predicts that plants maximize their growth by allocating biomass between resource uptake organs, such as shoot and roots, so that growth is equally limited by all resources (Bloom et al., 1985; Tilman, 1988; Aikio and Markkola, 2002). This implies that plants should increase allocation to shoots when light is more limiting than nutrients, and to roots when nutrients are more limiting than light. As the availability of resources varies between seasons, as well as along successional gradients and relative to plant size, we can expect to see variation in the extent that different resources limit plant growth. This can be expected to favour phenotypic plasticity in resource uptake rates or in the ability to buffer against resource changes by means of internal resource storage. In the context of global warming, the overall decrease of availability of nutrient resources towards northern latitudes challenges the plasticity of host trees and their symbionts in nutrient uptake. Consistent with optimal use theory, biomass partitioning in forest trees shows latitudinal changes with generally higher relative allocation to fine roots in the north than in the south (Helmisaari et al., 2007). This is due to the short and cold growing season and soil podsolization leading to low nutrient availability. Thus, northern trees must allocate relatively more biomass to fine roots to support the nutritional needs of the foliage (Helmisaari et al., 2007). As an additional adaptation to low nutrient availability in the north, nutrient resorption from old needles was higher in pine populations originating from high latitudes (Oleksyn et al., 2003). However, it is not known to what extent allometric ratios in tree populations are genetically determined. In

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common garden experiments northern ecotypes had higher belowground biomass allocation and starch concentrations in fine roots than southern ecotypes (Oleksyn et al., 1999, 2000), implying at least a partial genetic control. On the other hand, light quality in the north may also strongly interact with belowground biomass allocation of trees. In laboratory experiments, enriched blue light, characteristic of night hours of the polar summer (Taulavuori et al., 2010), decreased root growth of micropropagated Prunus (Pinker et al., 1989) and Betula plants (Fuernkranz et al., 1990), while increased rooting under blue light has also been reported in Betula (Sæbø et al., 1995). The latter is consistent with findings of lower root biomass, and increased root elongation of a southern population of Scots pine under blue light removal (Sarala et al., 2011). However, such a response in root biomass was not observed in a northern population. It may be assumed that enriched blue light reactions in trees are generally reverse to reactions related to canopy shade: shade, depleted of blue wavelengths, decreases root to shoot ratio in understorey plants (Keuskamp et al., 2012). Resource partitioning between the tree host and EMF symbionts varies during a growing season. At the beginning of a growing season, photoassimilates are allocated to shoot height growth, while carbon flow is directed below ground to roots (Steinaker et al., 2012) and EMF growth (mycelia and sporocarps) towards the end of the season (Wallander et al., 2013; Högberg et al., 2010). Most of the carbon used by fungi is recently fixed, while stored carbon is mainly used by host plant functions. For example, EMF sporocarps are produced solely with currently assimilated carbon (Högberg et al., 2010; Teramoto et al., 2012), which can make EMF carbon economy responsive to changes in a host plant’s photosynthetic rate in different light environments. However, host trees with a free growth pattern show higher plasticity in their carbon allocation than those with fixed growth (Laurence et al., 1994), also in terms of root growth (Kalliokoski et al., 2007; Ostonen et al., 2013). This is further reflected in the growth rate of different species, as trees with a free growth pattern usually have a higher growth rate than those with a fixed growth pattern. Differential shoot and root growth patterns in fixed and free-growth trees may imply corresponding variability in the seasonal carbon flux to EMF symbionts. Although a high variation in root phenology may occur among species with different growth rates and patterns and even between years (Steinaker et al., 2012; McCormack et al., 2014), some general trends have been found. Thus, while shoot growth of slowly-growing host trees occurs mainly during the early growing season, their root growth has been found to start later than in rapidly growing host trees (Lyr and Hoffmann, 1967; McCormack et al., 2012, 2014). Moreover, McCormack et al. (2014) suggest that host trees associated with EMF fungi may show a later root growth peak than those with AM fungi. Different types of host trees, in terms of growth pattern and rate and mycorrhizal association, may thus offer temporally different carbon resources for fungal communities. It is challenging to make predictions on belowground biomass allocation, nutrient availability and interactions with EMF symbionts under northward range shifts of tree populations. Soil temperatures will increase with global warming, which may enhance root growth. On the other hand, soil warming will also increase N mineralization and further lead to higher nutrient availability in the northern soils, thus decreasing the need for high investments to nutrient-acquiring organs. It is therefore not surprising that contradictory results have been found in warming experiments. Thus, long-term soil warming led to higher EMF living biomass in Betula nana (Clemmensen et al., 2013; Deslippe et al., 2011), while in Picea mariana EMF abundance decreased (Allison and Treseder, 2008). However, impaired growth of plants from southern ecotypes under polar summer conditions may

further cause negative impacts on EMF and interfere with nutrient uptake. During a northward range shift tree populations would also have to adapt to local EMF symbiont pools. EMF species richness is very high, including generalist fungi with low host specificity and specialists associating only with certain host tree genera. Arctic EMF have been suggested to possess low specificity in terms of host choice (Ryberg et al., 2009; Timling et al., 2012). Therefore, tree populations will most likely find compatible EMF symbionts, especially since EMF show very long-distance dispersal (Geml et al., 2012). The outcome of competition between southern host ecotypes and their EMF and original northern hosts associated with local EMF communities is difficult to predict. 5. Key questions The main objective in our review is to synthesise existing knowledge and highlight research needs and methodological approaches to predict the performance of southern host trees and their EMF symbionts in northern light conditions, where climate change is expected to expand their future range. We aim to combine recent advances in understanding the role of light environment under global warming conditions, and consequent species’ and populations’ range shifts towards the north, with the recent advances in molecular identification techniques for EMF community composition. We draw our predictions under the assumption that (1) global warming will lead to range shifts of the host towards a more northern light climate (ACIA, 2005; Taulavuori et al., 2010; Saikkonen et al., 2012; Taulavuori, 2013) and that (2) cessation of shoot height growth of tree hosts is regulated by day length. Therefore, growth cessation of the host may be delayed in latitudes higher than those of the host origin. Moreover, differences in the starting of C allocation belowground between host trees with a fixed or free growth pattern may lead to different responses of associated EMF communities along with changing light environment. Such implications have been found along with global warming, as EMF sporocarp phenology has been found to be delayed in forest sites dominated by deciduous tree hosts but not those with coniferous hosts (Gange et al., 2007). It is well-documented that carbon allocation from host trees drives EMF fungal biomass and communities belowground, and shapes EMF communities associated with forest trees (Saikkonen et al., 1999; Kuikka et al., 2003; Tarvainen et al., 2003; Markkola et al., 2004; Cudlin et al., 2007; Saravesi et al., 2008, 2015; Andrew and Lilleskov 2009; Ruotsalainen et al., 2009). In contrast, except for UV and far-red parts of the spectrum (see e.g. de la Rosa et al., 1998, 2003) impacts of light quality have largely been neglected in the context of EM fungal symbiosis. Predicted shifts of ranges of southern forest tree species and photoperiodic ecotypes will bring these trees to a more northern light environment, which may lead to conflicts between the day-length-driven growth of the southern-origin hosts and EMF symbionts in a northern light environment. This may lead to novel allocation patterns in host– symbiont relationships. Since root-associated fungi are crucial in carbon sequestration in soils (Clemmensen et al., 2013) and changes in host carbon flux to EMF may drastically change the rate of carbon cycling in subarctic forest ecosystems (Kaukonen et al., 2013), any major change in carbon allocation between the tree host and EMF symbionts is of importance. Against this background, we assume that: 1. Resource partitioning between boreal tree hosts and EMF symbionts is driven by light intensity, quality and duration (day length) 2. Seasonality of C flux belowground is dependent on the growth pattern and plasticity of biomass allocation of the host species and its locally adapted photoperiodic ecotype

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3. Changes in EMF communities are based on varying C demands of the fungi and varying C costs for the host in a changing environment We further hypothesize: 1. Carbon allocation to roots and EMF in different host species and locally adapted photoperiodic ecotypes will respond differentially to northern light climate, especially to photoperiod and proportionally higher diffuse blue light 2. Since carbon flux belowground may start later in northwardshifted southern populations in the autumn, also mycelial growth and reproduction in the EMF associated with southern populations could occur later. This may also lead to changes in fungal community composition 3. EMF phenology and community composition may show different responses to a changing light climate when associated with host trees of fixed or free growth pattern 4. Responses of EMF symbionts associated with locally adapted host populations vary; this may lead to changes in EMF communities 5. Moreover, as EMF fungi vary in host choice, generalist EMF are assumed to perform better during host range shift than EMF highly specialized to a certain host species, as host switching may not be possible in the latter case

6. Experimental approach possibilities The traditional common garden experiment system (CGE; i.e. different populations transplanted and grown on the same site) may be valuable in studying biomass partitioning between EMF and hosts of different tree species and their locally light adapted ecotypes. Information on genetic control of trees on belowground allocation is surprisingly scarce. Generally, allocation to root growth in trees is increased towards the north (Oleksyn et al., 1999; Helmisaari et al., 2007; Ostonen et al., 2011) and is thus likely to be higher in northern ecotypes. The questions requiring experimental studies include the degree of belowground allocation to roots and, consequently, to mycorrhizal fungi determined by tree provenance. The manipulation of belowground carbon allocation can be achieved through nitrogen fertilization, which typically directs allocation from roots to shoots. Also, nitrogen levels in live and senescing tree leaves can be studied through fertilization experiments, as this changes nutrient resorption rate that is expected to be more efficient in northern compared to southern tree populations (Oleksyn et al., 2003). This may further interact with belowground allocation patterns in tree provenances. Traditional CGEs, however, have certain limitations when related to a warming climate. Given that the temperature is the most important ecological filter for the formation of vegetation zones in the north (Taulavuori, 2013; and references therein), the CGE system is unrealistic: it is based on range shifts both from south-to-north and vice versa, whereas the climate change is characteristically directional, driving vegetation mainly towards the north. In principle, any experiment that is based on the ‘transfer of the southern climate towards the north’ may provide a more sophisticated update to CGEs and hence produce novel data. The goal is to mimic range shift conditions due to global warming, and thereby compare reaction norms in key traits between southern (colonizing) and northern (local) populations and species (Taulavuori 2013). Basically, mini-greenhouses that do not affect light conditions, and are equipped with heating systems to follow the temperature at a southern latitude location in real time may provide an optimal experimental infrastructure.

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Additional information may be obtained by light manipulation experiments. They may be based on either light exclusion by filtering chambers (e.g. Taulavuori et al., 2005; Sarala et al., 2007, 2011), or light inclusion by lamp systems (Taulavuori et al., 2013). In the latter case, the LEDs (light emitting diodes) provide a variety of possibilities to construct the desired light spectrum. Finally, phytotron experiments are classically used to manipulate changes in photoperiod (Taulavuori et al., 2000). 7. Potential modelling approaches Finally, data obtained from experimental studies with varying light quality may be used for modelling of host plant and symbiont growth, which may in turn affect species competitive ability and distribution. The functional response of plant growth to essential resources, especially to light and nitrogen, is relatively well studied, which gives a solid basis for using, e.g. Michaelis–Menten relationship between availability and rate of acquisition (Aikio and Markkola, 2002). The growth of shoot and roots increases the potential uptake rate of light and nutrients, respectively, and the optimal allocation theory (Bloom et al., 1985) predicts that plants increase the relative allocation to the organ that takes up the more limiting resource. On the other hand, plants may also be opportunistic in resource acquisition and biomass partitioning, e.g. by producing a more dense foliage and thicker leaves when in good availability of light and increasing fine root proliferation in those patches of soil where nutrient concentration is highest. The maintenance of stoichiometric balance under opportunistic resource uptake requires the ability to store excess resources for later use, which stabilizes the long-term resource status and allows for the long-term uptake rate to converge with the predicted equal limitation by each resource. Mycorrhizal symbionts typically affect both host plant nutrient acquisition rate and carbon expenditure, thereby affecting the shape and parametrization of plant growth models (Aikio and Ruotsalainen, 2002). An increase in nutrient uptake rate brought about by mycorrhizal fungi will bear higher carbon costs, thereby changing the relative limitation of plant growth by light and nutrients and changing the optimal allocation of plant growth between shoot and roots (Aikio and Markkola, 2002). This can be addressed through a model where plant growth is a function of availability and interaction between light and nutrients, as well as the biomass of the mycorrhizal fungi that is in demand of plant photosynthates. In general terms, the dynamics of plant (P) and mychorrhizal fungus (M) biomass can be modelled as a function of maximum plant growth rate (r), which is restricted by the availability and mycorrhizal provision of resources (X) to the plant at the rate f(X,M) and carbon expenditure to mycorrhizal symbionts at the rate g(P,M). With the addition of the biomass maintenance costs (m), plant growth rate can be expressed as: dP ¼ rPf ðX;MÞ  gðP;MÞ  mP dt Ideally, the growth model would be constructed before the experimental studies, in order to ascertain that the planned study will yield the required parameter estimates. Some of the required data, or even previously estimated parameters, may be available in published literature, but the growth function f(X,M) is the most critical component, as it links plant growth to the other components of the system, namely resource availability and the biomass of the symbiotic partner. A fully parameterized model would allow quantitative predictions on plant biomass at different conditions, but the data, and resources for its acquisition, will often fall short of reaching this goal. It is therefore necessary to concentrate experimental

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parametrization efforts on the functional response f(X,M) that is the most important part of the model. The comparison of the functional response functions between species already gives valuable information on the performance of species in a new environment. Specifically, the growth model can be analysed for the optimal allocation between shoot and roots, as well as allocation to the mycorrhizal fungi at different light quantity and quality, as well as nutrient conditions. This modelling approach could be adapted to light quality changes due to range shifts of forest trees. The difference in day length and spectral quality of light in the north and south will shape the functional response of plant growth to light. The analysis of the model will yield predictions for various scenarios or environments plants have to face when shifting their ranges under climate change. In addition to modelling the effect of environmental conditions, revealing comparisons can be made between plants of variable growth patterns. For example, we can expect that the shape of the functional response differs between trees showing different phenotypic plasticity in biomass allocation (Laurence et al., 1994; Kalliokoski et al., 2007; Ostonen et al., 2013) and having either a fixed growth pattern (such as Pinus sylvestris) or free growth pattern (e.g. Betula pendula). These ectomycorrhizal forest tree species are therefore suitable model species for testing various model predictions. The host plants have usually been the focus of studies on mycorrhizal symbionts and the biomass dynamics of the fungal partner of the system is relatively poorly known. In modelling terms, this would require experimental studies on the relationship between carbon expenditure to mycorrhizal fungi g(P,M) and the growth rate of fungal biomass dM/dt. The simplest assumption is that the relationship is mediated by a constant resource use efficiency (c), which translates the carbon allocation to fungal growth rate. With the addition of a combined term for the hyphal maintenance costs and rate of senescence (s), the mycorrhizal biomass becomes donor controlled by plant biomass: dM ¼ cgðP; MÞ  sM dt Some mycorrhizal fungi have a degree of saprophytic functions, i.e. production of hydrolytic enzymes, but they generally require a host for supplying metabolic carbon (Lindahl and Tunlid, 2015). The dependency of mycorrhizal fungi on their host plants is demonstrated in natural and experimental defoliation of host plants (Kuikka et al., 2003; Markkola et al., 2004; Saravesi et al., 2008, 2011, 2015; Ruotsalainen et al., 2009), which have led to a strong decline in the abundance of mycorrhizal fungi and an increase of saprophytic fungi. In our modelling framework, defoliation leads to a marked decrease in the flow of carbon from plant to mycorrhiza (term g(P,M)), which will lead to a decrease in fungal biomass. The detailed shape of the functional response of fungi to host plants may require isotope markers or other means of following the path of plant photosynthates to fungi. Although such methods have demonstrated the flow of carbon from plants to fungi, quantitative applications have so far been rare. However, we can expect that methodological advances in the future will yield better data for modelling purposes and permit in situ tests of predictions that are currently confined to controlled laboratory environments. 8. Conclusions We suggest that under host tree range shifts, different host tree species and their locally adapted photoperiodic ecotypes will respond differentially to the northern light climate in terms of their C allocation to roots and fungal symbionts. This is due to changes in

phenology of C flux belowground, varying C demands of different fungal symbionts and differences in host tree growth patterns and rates. We assume generalist EMF to perform better during host range shifts. Experimental work on responses of different host trees and their fungal symbionts to varying light environments will be conducted, and the results will be used for the modelling of host tree growth and their fungal symbionts encountering a range shift towards the northern light climate. The response of fungal communities will be part of the ecological competition between different northern populations, which have to adapt to changing temperature, and southern populations, which have to adapt to a changing light environment, as well as disperse to the north. As the northern populations are already inhabiting the competitive site as mature individuals and southern populations have to colonize the area via seed dispersal, we can expect that northern populations have at least an initial advantage in competition. Competition between different populations may have a more even outset when it takes place between forest trees that are planted or sown on sites that are free of existing vegetation and begin their growth at the same size. It is likely that fungal symbionts have play a more decisive role in such conditions, since other differences between populations are to a large extent factored out. Acknowledgements We thank the Academy of Finland for funding of the projects #278364, #133889 and #138309, and M.Sc. Aaron Bergdahl for linguistic revision. References ACIA, 2005. Arctic Climate Impact assessment. University Press, Cambridge, pp. 1042. Aikio, S., Markkola, A.M., 2002. Optimality and phenotypic plasticity of shoot-toroot ratio under variable light and nutrient availaiblity. Evol. Ecol. 16, 67–76. Aikio, S., Ruotsalainen, A.L., 2002. The modelled growth of mycorrhizal and nonmycorrhizal plants under constant vs. variable soil nutrient concentration. Mycorrhiza 12, 257–261. Aikio, S., Duncan, R.P., Hulme, P.E., 2010. Lag-phases in alien plant invasions: separating the facts from the artefacts. Oikos 119, 370–378. Allison, S.D., Treseder, K.K., 2008. Warming and drying suppress microbial activity and carbon cycling in boreal forest soils. Global Change Biol. 14, 2892–2909. Andrew, C., Lilleskov, E.A., 2009. Productivity and community structure of ectomycorrhizal fugal sporocarps under increased atmospheric CO2 and O3. Ecol. Lett. 12, 813–822. Bazzaz, F.A., 1990. The response of natural ecosystems to rising global CO2 levels. Annu. Rev. Ecol. Syst. 21, 167–196. Bloom, A.J., Chapin III, F.S., Mooney, H.A., 1985. Resource limitation in plants–an economic analogy. Annu. Rev. Ecol. Syst. 16, 363–392. Cashmore, A.R., 2006. Cryptochromes, In: Schäfer, E., Nagy, F. (Eds.), Photomorphogenesis in Plants and Bacteria: Function and Signal Transduction Mechanisms. 3rd ed. Springer, Dordrecht, Netherlands, pp. 199–221. Clemmensen, K.E., Bahr, A., Ovaskainen, O., Dahlberg, A., Ekblad, A., Wallander, H., Stenlid, J., Finlay, R., Wardle, D.A., Lindahl, B.D., 2013. Roots and associated fungi drive long-term carbon sequestration in boreal forest. Science 339, 1615–1618. Cudlin, P., Kieliszewska-Rokicka, B., Rudawska, M., Grebenc, T., Alberton, O., Lehto, T., Bakker, M.R., Borja, I., Konopka, B., Leski, T., Kraighter, H., Kuyper, T.W., 2007. Fine roots and ectomycorrhizas as indicators of environmental change. Plant Biosyst. 141, 406–425. de la Rosa, T.H., Aphalo, P.J., Lehto, T., 1998. Effects of far-red light on the growth, mycorrhiza and mineral nutrition of Scots pine. Plant Soil 201, 17–25. de la Rosa, T.H., Aphalo, P.J., Lehto, T., 2003. Effects of ultraviolet-B radiation on growth, mycorrhizas and mineral nutrition of silver birch (Betula pendula) seedlings grown in low-nutrient conditions. Global Change Biol. 9, 65–73. Deslippe, J.R., Hartmann, M., Mohn, W.W., Simard, S.W., 2011. Long-term experimental manipulation of climate alters the ectomycorrhizal community of Betula nana in Arctic tundra. Global Change Biol. 17, 1625–1636. Dosskey, M.G., Linderman, R.G., Boersma, L., 1990. Carbon-sink stimulation of photosynthesis in Douglas fir seedlings by some ectomycorrhizas. New Phytol. 115, 269–274. Finlay, R., Söderström, B., 1992. Mycorrhiza and carbon flow to the soil. In: Allen, M.J. (Ed.), Mycorrhizal Functioning. Chapman & Hall, New York, pp. 134–160. Fuernkranz, H.A., Nowak, C.A., Maynard, C.A., 1990. Light effects on in vitro adventitious root formation in axillary shoots of mature Prunus serotina. Physiol. Plant. 80, 337–341.

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